Rhythmicity of coastal marine picoeukaryotes, bacteria and archaea despite irregular environmental perturbations Stefan Lambert, Margot Tragin, Jean-Claude Lozano, Jean-François Ghiglione, Daniel Vaulot, François-Yves Bouget, Pierre Galand To cite this version: Stefan Lambert, Margot Tragin, Jean-Claude Lozano, Jean-François Ghiglione, Daniel Vaulot, et al.. Rhythmicity of coastal marine picoeukaryotes, bacteria and archaea despite irregular environmental perturbations. ISME Journal, Nature Publishing Group, 2019, 13 (2), pp.388-401. 10.1038/s41396- 018-0281-z. hal-02326251 HAL Id: hal-02326251 https://hal.archives-ouvertes.fr/hal-02326251 Submitted on 19 Nov 2020 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Rhythmicity of coastal marine picoeukaryotes, bacteria and archaea despite irregular environmental perturbations Stefan Lambert, Margot Tragin, Jean-Claude Lozano, Jean-François Ghiglione, Daniel Vaulot, François-Yves Bouget, Pierre Galand To cite this version: Stefan Lambert, Margot Tragin, Jean-Claude Lozano, Jean-François Ghiglione, Daniel Vaulot, et al.. Rhythmicity of coastal marine picoeukaryotes, bacteria and archaea despite irregular environmental perturbations. ISME Journal, Nature Publishing Group, 2019, 13 (2), pp.388-401. 10.1038/s41396- 018-0281-z. hal-02326251 HAL Id: hal-02326251 https://hal.archives-ouvertes.fr/hal-02326251 Submitted on 19 Nov 2020 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Rhythmicity of coastal marine picoeukaryotes, bacteria and archaea despite irregular environmental perturbations 1 ● 2 ● 1 ● 1 ● 2 ● Stefan Lambert Margot Tragin Jean-Claude Lozano Jean-François Ghiglione Daniel Vaulot 1 ● 3 François-Yves Bouget Pierre E. Galand Received: 25 May 2018 / Revised: 20 August 2018 / Accepted: 26 August 2018 Abstract Seasonality in marine microorganisms has been classically observed in phytoplankton blooms, and more recently studied at the community level in prokaryotes, but rarely investigated at the scale of individual microbial taxa. Here we test if specific marine eukaryotic phytoplankton, bacterial and archaeal taxa display yearly rhythms at a coastal site impacted by irregular environmental perturbations. Our seven-year study in the Bay of Banyuls (North Western Mediterranean Sea) shows that despite some fluctuating environmental conditions, many microbial taxa displayed significant yearly rhythms. The robust rhythmicity was found in both autotrophs (picoeukaryotes and cyanobacteria) and heterotrophic prokaryotes. Sporadic meteorological events and irregular nutrient supplies did, however, trigger the appearance of less common non-rhythmic 1234567890();,: 1234567890();,: taxa. Among the environmental parameters that were measured, the main drivers of rhythmicity were temperature and day length. Seasonal autotrophs may thus be setting the pace for rhythmic heterotrophs. Similar environmental niches may be driving seasonality as well. The observed strong association between Micromonas and SAR11, which both need thiamine precursors for growth, could be a first indication that shared nutritional niches may explain some rhythmic patterns of co- occurrence. Introduction migrations in animals, flowering in plants and blooms in plankton communities [1–3]. Phytoplanktonic blooms in Regular and predictable fluctuations of environmental temperate oceanic areas are a typical example of seasonal parameters have a great impact on life. Seasonality sets the events. Several classical theories, from Sverdrup’s “Critical pace for many reoccurring life events, such as mating or Depths Hypothesis” [4] to Behrenfeld’s “Dilution-Recou- pling Hypothesis” [5], have attempted to explain the mechanisms triggering bloom formation. However, these theories do not aim to explain the reoccurrence and sea- Electronic supplementary material The online version of this article sonality of specific microbial taxa. In macroscopic organ- (https://doi.org/10.1038/s41396-018-0281-z) contains supplementary fi material, which is available to authorized users. isms, seasonality results from a ne interplay between external environmental factors and the internal circadian * François-Yves Bouget clock, which is an endogenous timekeeper [6]. In marine [email protected] microorganisms, circadian rhythms are less well known and * Pierre E. Galand they have been reported only in cyanobacteria and in some [email protected] eukaryotic microalgae [7–10]. However, the effect of environmental forcing on the seasonality of entire bacterial 1 ’ CNRS, Laboratoire d Océanographie Microbienne (LOMIC), communities has been studied more extensively and reoc- Observatoire Océanologique de Banyuls, Sorbonne Université, Banyuls sur Mer, Paris, France curring microbial communities are often observed 2 responding to environmental changes [11–15]. CNRS, UMR7144, Station Biologique de Roscoff, Sorbonne fl Université, Roscoff, Paris, France Oceans are uctuating habitats that are often marked by a strong seasonality. These regular environmental changes 3 CNRS, Laboratoire d’Ecogéochimie des Environnements Benthiques (LECOB), Observatoire Océanologique de Banyuls, allow for an overall high microbial community diversity, Sorbonne Université, Banyuls sur Mer, Paris, France since the environment can accommodate different species in S. Lambert et al. the same space, but at different times of the year [16]. factors that could contribute to microbial seasonality. We Within a year, diversity also varies locally with peaks also used statistical tools to quantify the rhythmicity of the observed in winter at high latitudes [15, 17] and community picoplankton and to detect patterns of co-occurrence composition changes with seasons. Seasonal cycles in between eukaryotic picophytoplankton (less than 3 µm), abiotic and/or biotic factors drive these community changes bacteria and archaea. [18, 19]. To understand the seasonality of marine microbial communities, several long term sampling sites have been established within the last couple decades leading to some Materials and methods important findings on the seasonality of major microbial groups in the surface of the ocean [14, 20–23] and the Environmental sampling reoccurring patterns of microbial community composition [12, 24]. Surface seawater (3 m depth) was collected roughly every Most of earlier studies focused on bacteria and there are 2 weeks from October 2007 to January 2015 at the Service only few reports on the seasonality of the other domains of d’Observation du Laboratoire Arago (SOLA) sampling life. For marine archaea, it has been shown that both rare station (42°31′N, 03°11′E) in the Bay of Banyuls-sur-Mer, and abundant members of the community were re-occurring North Western Mediterranean Sea, France. Seawater was seasonally and that different ecotypes of archaea had dif- collected in 10 l Niskin bottles and then kept in 10 l carboys ferent seasonal patterns [20, 25]. For phytoplankton, evi- until arrival to the laboratory within one hour. A subsample dence for global patterns of temporal dynamics were of 5 l was prefiltered through 3 μm pore-size polycarbonate obtained by compiling seasonal data of chlorophyll a con- filters (Merck-Millipore, Darmstadt, Germany), and the centrations [26]. Molecular techniques also revealed that microbial biomass was collected on 0.22 μm pore-size GV microbial eukaryote assemblages displayed seasonality Sterivex cartridges (Merck-Millipore) and stored at –80 °C patterns in surface marine waters [27, 28], but interestingly until nucleic acid extraction. not always in the deeper ocean [28]. Reports on the sea- For cytometry, unfiltered seawater samples were fixed at sonality of archaea and eukaryotes are scarce, but there are a final concentration of 1% glutaraldehyde, incubated for even fewer time series studies covering simultaneously the 15 min at ambient temperature in the dark, frozen in liquid three domains of life. Steele et al. [29] identified the nitrogen and stored at −80 °C. Cytometry analyses were microorganisms that co-occurred during a 3-year study at performed on a Becton Dickinson FacsCalibur. Cells were the SPOT station (Southern California, USA). At the same excited at 488 nm and discriminated by SSC and red site, a 21-day study of the dynamics of phytoplankton, fluorescence (measured at 670 nm; chlorophyll content). archaea and bacteria revealed a rapid succession of micro- Orange fluorescence (measured at 585 ± 21 nm), produced bial species during a bloom [30], which highlighted the by phycoerythrin, was used to discriminate Synechococcus importance of